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An Evaluation of the Nontarget Effects of Transgenic Bacillus Thuringiensis Maize on Arbuscular Mycorrhizal Fungi in the Soil Ecosystem

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An Evaluation of the Nontarget Effects of Transgenic Bacillus Thuringiensis Maize on Arbuscular Mycorrhizal Fungi in the Soil Ecosystem Portland State University PDXScholar Dissertations and Theses Dissertations and Theses Summer 8-1-2013 An Evaluation of the Nontarget Effects of Transgenic Bacillus thuringiensis Maize on Arbuscular Mycorrhizal Fungi in the Soil Ecosystem Tanya Elizabeth Amy Cheeke Portland State University Follow this and additional works at: https://pdxscholar.library.pdx.edu/open_access_etds Part of the Food Biotechnology Commons, Molecular, Genetic, and Biochemical Nutrition Commons, and the Other Genetics and Genomics Commons Let us know how access to this document benefits ou.y Recommended Citation Cheeke, Tanya Elizabeth Amy, "An Evaluation of the Nontarget Effects of Transgenic Bacillus thuringiensis Maize on Arbuscular Mycorrhizal Fungi in the Soil Ecosystem" (2013). Dissertations and Theses. Paper 1027. https://doi.org/10.15760/etd.1027 This Dissertation is brought to you for free and open access. It has been accepted for inclusion in Dissertations and Theses by an authorized administrator of PDXScholar. Please contact us if we can make this document more accessible: [email protected]. An Evaluation of the Nontarget Effects of Transgenic Bacillus thuringiensis Maize on Arbuscular Mycorrhizal Fungi in the Soil Ecosystem by Tanya Elizabeth Amy Cheeke A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology Dissertation Committee: Mitchell B. Cruzan, Chair Todd Rosenstiel Lisa Weasel Daniel Ballhorn James Bever William Fish Portland State University 2013 © 2013 Tanya Elizabeth Amy Cheeke Abstract My dissertation research examined the effect of the cultivation of insect-resistant Bacillus thuringiensis (Bt) maize on the soil environment with a goal of understanding how to obtain a balance between technological advancement and maintenance of a healthy soil ecosystem. Although Bt plants may help to reduce pesticide use, conferring benefits to farm workers and the environment, there are still unresolved questions about how the cultivation of Bt plants affects soil organisms. For this dissertation project, I used 14 different genotypes of Bt maize and non-Bt maize (Zea mays) to investigate the effects of transgenic Bt plants on the colonization ability, abundance, and diversity of symbiotic arbuscular mycorrhizal fungi (AMF) in the soil ecosystem over time. My greenhouse studies demonstrated that Bt maize plants exhibited reduced AMF colonization across multiple Bt genotypes and that effects were most pronounced when fertilizer levels were limited and spore density was high. In addition, I found that although differences in AMF colonization between Bt and non-Bt maize were difficult to detect in the field, spore density was reduced in Bt field plots after just one growing season. When I tested the effect of plot history on AMF and plant growth, I found that Bt and non-Bt maize plants had higher leaf chlorophyll content when grown in plots previously cultivated with the same maize line as the previous year, indicative of a positive feedback effect. I also examined potential mechanisms contributing to the reduced AMF colonization observed in Bt maize in greenhouse studies and determined that follow-up experiments should continue to investigate differences in root apoplastic invertase activity and root i permeability in Bt and non-Bt maize. Future investigations would also benefit from examining potential differences in root exudate profiles and volatile organic compounds between Bt and non-Bt cultivars. Taken together, my dissertation results suggest that, while difficult to detect in the field, reductions in AMF colonization in Bt maize roots may be ecologically significant as they could lead to a decrease in the abundance of AMF propagules in the soil over time, potentially impacting soil structure and function in areas where Bt crop cultivation is high. ii Dedication Dedicated to my parents, soil ecologists everywhere, and students who have worked hard to achieve their dreams iii Acknowledgments I am grateful for the many people who helped me over the course of this dissertation project and for the funding agencies that supported this research. I would like to thank Carol A. Miles, Mike Beug, Pat Labine, and my colleagues in the Ecological Agriculture program at The Evergreen State College for introducing me to the science of sustainable agriculture and for inspiring me to pursue this dissertation work. At Portland State University (PSU), I have benefited tremendously from the wonderful people on my committee who have guided me, nurtured me, challenged me, and advised me through this entire process. Mitch Cruzan, my primary advisor and the fearless leader of our lab has taught me more than I could ever list here. He has been my greatest cheerleader and invited me into his lab when I was a new student with just an idea about investigating the nontarget effects of genetically modified crops on soil organisms. Without him, this project may never have gotten off the ground. Lisa Weasel has been an inspiration to me in the academic realm and I am grateful for her valuable perspective on genetically modified crops which has helped to shape my research questions. Todd Rosenstiel has a vast breadth of knowledge and always provides insightful and thought-provoking comments on my work that I have been able to learn and grow from. Jim Bever is another member of my committee who I have learned so much from. He adopted me into his mycorrhizal lab at Indiana University where I gained skills in statistical analysis, bioinformatics, and molecular biology, and his lab is also the place where I’ve formed some of my strongest friendships. I am so grateful for his advice, guidance, and friendly iv manner that has helped guide me through the last few years of my graduate career. Daniel Ballhorn has provided me with valuable perspectives on tri-trophic interactions in a variety of plant species and I learned a lot from his chemical ecology reading group. Hap Pritchard, a former member of my committee, provided assistance with the design of this project in its early stages. I am also thankful for all the members of the Cruzan lab who have helped me with this project over the years including Kristin Anton, Paul Sochacki, Heather Machado, Trieste Musial, Alisa Ramakrishnan, Gina Marchini, Laura Taylor, Kevin Weitemier, Caitlin Lee, and Rachael Workman as well as fellow graduate students Melissa DeYoung, Sara Viernum, and Geoff Diemer. I have also benefited from the help of many amazing undergraduates, post-baccs, high school students, and volunteers in the lab including the “myco-boys” Brian Pace, Corey Guidry, and Matt LaPlante, as well as Luke Reyes, Hayley Darby, Danielle Butler, Belma Hergic, Scott Kiel, Dan Kowalkiewicz, Courtney Crawford, Kiernan Garrett, Alessandra Elliott, Erik Hasenkopf, Ann Rasmussen, Jennifer Jones, Hilary Miller, Sarah Arteaga, Sarah Gabriel, Madeline Steele, Melia Chase, Sage Wagner, Emily Fielding, and many others who helped with corn harvesting, processing, and slide-making during those long, hot days of summer. I would also like to thank the helpful people in the PSU Department of Biology, especially members of the biology office Leah Tuor, Autumn Droste, Sinnamon Tierney, and Amy Jolsted, the prep room staff Jane Boone and Lindsay Henderson, as well as the greenhouse managers Lane Greer and Linda Taylor. At Indiana University, I received research training, advice, comments on my book chapter, and help with statistical v analysis from Jim Bever, Peggy Schultz, Ursel Schuette, Wittaya Kaonongbua, Jeremiah Henning, Liz Koziol, Tom Platt, Anna Rosling, Rich Phillips, Chris Hemmerich, and Wesley Beaulieu. Joe Morton at INVAM helped me identify mycorrhizal spores from my field site and has always been a great resource for all things mycorrhizae. Bill Landesman, Nancy C. Johnson, David Coleman, Diana Wall, and other members of the Ecological Society of America Soil Ecology Section helped me put together the 2009 ESA symposium from which the book I edited, Microbial Ecology in Sustainable Agroecosystems, was derived. I would also like to thank my family -- Mom, Dad, Robert, Ryan, and Clarke, and my friends Kelly Owen, Chris Dean, Cassandra Hoy, and Halo for assisting me with field work and for helping to processing root samples when it was late, hot, and we still had hundreds of plants to go. I would also like to thank my wonderful partner Neal for all of his love, patience, and support during my graduate studies and for helping me process root samples, even on the weekends and after he’d already worked a long day at his own job. Finally, I’d like to acknowledge my funding sources, without which I never could have done this work. Funding for this research was provided by the PSU Forbes Lea Foundation, PSU Scholarly and Creative grants to Brian Pace and Matt LaPlante for their work on this project, the Charles A. and Anne Morrow Lindbergh Foundation, Environmental Protection Agency Science to Achieve Results Fellowship, Botanical Society of America, Sigma Xi, The National Science Foundation, Sigma Delta Epsilon-Graduate Women in Science, and travel grants from The Ecological Society of America, PSU Biology Graduate Student Association, Botanical Society of America, vi Marie Brown Travel Grant, and a Miller Sustainability Travel Award. vii Table of Contents Abstract ................................................................................................................................ i Dedication .........................................................................................................................
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